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Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

Baker CA, Huck KR, Carlson BA - Elife (2015)

Bottom Line: We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform.These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies.Our findings provide the first evidence for sensory coding through oscillatory synchrony.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Washington University in St. Louis, St. Louis, United States.

ABSTRACT
Adaptations to an organism's environment often involve sensory system modifications. In this study, we address how evolutionary divergence in sensory perception relates to the physiological coding of stimuli. Mormyrid fishes that can detect subtle variations in electric communication signals encode signal waveform into spike-timing differences between sensory receptors. In contrast, the receptors of species insensitive to waveform variation produce spontaneously oscillating potentials. We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform. These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies. Thus, different perceptual capabilities correspond to different receptor physiologies. We hypothesize that these divergent mechanisms represent adaptations for different social environments. Our findings provide the first evidence for sensory coding through oscillatory synchrony.

No MeSH data available.


Spiking and oscillating receptors encode interpulse intervals into interspike and interoscillation intervals, respectively.(A, B) Extracellular recording from a spiking receptor in B. niger in response to a pair of positive-polarity monopolar square pulses of 0.2-ms duration and 3.0-ms interpulse interval (IPI) (A) and 0.30-ms IPI (B). A spike occurred in response to the first pulse only for the 0.30-ms IPI. Stimulus artifacts were removed from recordings for clarity. (C) The probability that a receptor fired spikes to both positive-polarity pulses in a pair vs IPI for spiking receptors from three species. (D) Interspike interval vs positive-polarity IPIs for the same spiking receptors shown in C. The receptors of P. adspersus and P. microphthalmus did not fire spikes in response to both pulses when IPIs were shorter than 1 ms, so there are no data points at these intervals. (E) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a single pulse (top) and to a pair of pulses with 3.0-ms IPI (bottom). Responses to each stimulus presentation are shown in gray and the average across stimulus presentations is shown in black. The interoscillation interval was defined as the time interval between the first poststimulus oscillatory peak evoked by the single pulse and that evoked by the second pulse in the pair and was measured from the averaged traces. (F) Same as E for 0.30-ms IPI. (G) Interoscillation interval vs IPI for the responses of P. tenuicauda receptors to positive-polarity stimuli. Each point in C, D, and G represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.007
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fig5: Spiking and oscillating receptors encode interpulse intervals into interspike and interoscillation intervals, respectively.(A, B) Extracellular recording from a spiking receptor in B. niger in response to a pair of positive-polarity monopolar square pulses of 0.2-ms duration and 3.0-ms interpulse interval (IPI) (A) and 0.30-ms IPI (B). A spike occurred in response to the first pulse only for the 0.30-ms IPI. Stimulus artifacts were removed from recordings for clarity. (C) The probability that a receptor fired spikes to both positive-polarity pulses in a pair vs IPI for spiking receptors from three species. (D) Interspike interval vs positive-polarity IPIs for the same spiking receptors shown in C. The receptors of P. adspersus and P. microphthalmus did not fire spikes in response to both pulses when IPIs were shorter than 1 ms, so there are no data points at these intervals. (E) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a single pulse (top) and to a pair of pulses with 3.0-ms IPI (bottom). Responses to each stimulus presentation are shown in gray and the average across stimulus presentations is shown in black. The interoscillation interval was defined as the time interval between the first poststimulus oscillatory peak evoked by the single pulse and that evoked by the second pulse in the pair and was measured from the averaged traces. (F) Same as E for 0.30-ms IPI. (G) Interoscillation interval vs IPI for the responses of P. tenuicauda receptors to positive-polarity stimuli. Each point in C, D, and G represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.007

Mentions: Electric communication signals consist of the EOD produced at variable IPIs. Whereas the stereotyped EOD waveform can contain identifying information, such as species and sex, the IPIs convey behavioral state (see Carlson, 2002 for review). To investigate IPI coding in the three species with spiking receptors included in this study, we presented receptors with a pair of 0.2-ms duration monopolar square pulses at a range of IPIs (Figure 5A,B).10.7554/eLife.08163.007Figure 5.Spiking and oscillating receptors encode interpulse intervals into interspike and interoscillation intervals, respectively.


Peripheral sensory coding through oscillatory synchrony in weakly electric fish.

Baker CA, Huck KR, Carlson BA - Elife (2015)

Spiking and oscillating receptors encode interpulse intervals into interspike and interoscillation intervals, respectively.(A, B) Extracellular recording from a spiking receptor in B. niger in response to a pair of positive-polarity monopolar square pulses of 0.2-ms duration and 3.0-ms interpulse interval (IPI) (A) and 0.30-ms IPI (B). A spike occurred in response to the first pulse only for the 0.30-ms IPI. Stimulus artifacts were removed from recordings for clarity. (C) The probability that a receptor fired spikes to both positive-polarity pulses in a pair vs IPI for spiking receptors from three species. (D) Interspike interval vs positive-polarity IPIs for the same spiking receptors shown in C. The receptors of P. adspersus and P. microphthalmus did not fire spikes in response to both pulses when IPIs were shorter than 1 ms, so there are no data points at these intervals. (E) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a single pulse (top) and to a pair of pulses with 3.0-ms IPI (bottom). Responses to each stimulus presentation are shown in gray and the average across stimulus presentations is shown in black. The interoscillation interval was defined as the time interval between the first poststimulus oscillatory peak evoked by the single pulse and that evoked by the second pulse in the pair and was measured from the averaged traces. (F) Same as E for 0.30-ms IPI. (G) Interoscillation interval vs IPI for the responses of P. tenuicauda receptors to positive-polarity stimuli. Each point in C, D, and G represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.007
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Related In: Results  -  Collection

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fig5: Spiking and oscillating receptors encode interpulse intervals into interspike and interoscillation intervals, respectively.(A, B) Extracellular recording from a spiking receptor in B. niger in response to a pair of positive-polarity monopolar square pulses of 0.2-ms duration and 3.0-ms interpulse interval (IPI) (A) and 0.30-ms IPI (B). A spike occurred in response to the first pulse only for the 0.30-ms IPI. Stimulus artifacts were removed from recordings for clarity. (C) The probability that a receptor fired spikes to both positive-polarity pulses in a pair vs IPI for spiking receptors from three species. (D) Interspike interval vs positive-polarity IPIs for the same spiking receptors shown in C. The receptors of P. adspersus and P. microphthalmus did not fire spikes in response to both pulses when IPIs were shorter than 1 ms, so there are no data points at these intervals. (E) Extracellular recordings from an oscillating receptor in P. tenuicauda in response to a single pulse (top) and to a pair of pulses with 3.0-ms IPI (bottom). Responses to each stimulus presentation are shown in gray and the average across stimulus presentations is shown in black. The interoscillation interval was defined as the time interval between the first poststimulus oscillatory peak evoked by the single pulse and that evoked by the second pulse in the pair and was measured from the averaged traces. (F) Same as E for 0.30-ms IPI. (G) Interoscillation interval vs IPI for the responses of P. tenuicauda receptors to positive-polarity stimuli. Each point in C, D, and G represents the mean across receptors and error bars represent S.E.M.DOI:http://dx.doi.org/10.7554/eLife.08163.007
Mentions: Electric communication signals consist of the EOD produced at variable IPIs. Whereas the stereotyped EOD waveform can contain identifying information, such as species and sex, the IPIs convey behavioral state (see Carlson, 2002 for review). To investigate IPI coding in the three species with spiking receptors included in this study, we presented receptors with a pair of 0.2-ms duration monopolar square pulses at a range of IPIs (Figure 5A,B).10.7554/eLife.08163.007Figure 5.Spiking and oscillating receptors encode interpulse intervals into interspike and interoscillation intervals, respectively.

Bottom Line: We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform.These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies.Our findings provide the first evidence for sensory coding through oscillatory synchrony.

View Article: PubMed Central - PubMed

Affiliation: Department of Biology, Washington University in St. Louis, St. Louis, United States.

ABSTRACT
Adaptations to an organism's environment often involve sensory system modifications. In this study, we address how evolutionary divergence in sensory perception relates to the physiological coding of stimuli. Mormyrid fishes that can detect subtle variations in electric communication signals encode signal waveform into spike-timing differences between sensory receptors. In contrast, the receptors of species insensitive to waveform variation produce spontaneously oscillating potentials. We found that oscillating receptors respond to electric pulses by resetting their phase, resulting in transient synchrony among receptors that encodes signal timing and location, but not waveform. These receptors were most sensitive to frequencies found only in the collective signals of groups of conspecifics, and this was correlated with increased behavioral responses to these frequencies. Thus, different perceptual capabilities correspond to different receptor physiologies. We hypothesize that these divergent mechanisms represent adaptations for different social environments. Our findings provide the first evidence for sensory coding through oscillatory synchrony.

No MeSH data available.